Acta Biologica Marisiensis COMPARATIVE HISTOLOGICAL ...€¦ · Ribes nigrum (black currant) is a perennial shrub which grows in bushy places, groves (Ciocarlan, 2000). It is also

ABMJ 2019, 2(2): 5-14 DOI: 10.2478/abmj-2019-0006

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COMPARATIVE HISTOLOGICAL EVALUATION OF THE FRUIT OF RIBES NIGRUM

AND RIBES RUBRUM

Eszter LACZKÓ-ZÖLD1, Andrea KOMLÓSI2, Erzsébet VARGA1*, Nóra PAPP2

1Department of Pharmacognosy and Phytotherapy, George Emil Palade University of Medicine, Pharmacy,

Sciences and Technology of Targu Mures, Gh. Marinescu 38, 540139 Targu Mures, Romania 2Department of Pharmacognosy, University of Pécs, Rókus 2, 7624 Pécs, Hungary

*Correspondence:

Erzsébet VARGA

[email protected]

Received: 04 December 2019; Accepted: 12 December 2019; Published: 30 December 2019

Abstract: To complete the wide range of studies on chemical composition and pharmacological potential of

the fruit of Ribes nigrum and Ribes rubrum, this work aimed to perform a comparative morpho-anatomical characterization of the fruits of both species and complete previously records of black currant as frequently

studied species. Microslides of fruits were made with rotation microtome, and then cross sections were

stained with toluidine blue. Documentation and evaluation were carried out in microphotos. In R. rubrum,

the epidermis cells are ovoid to round, while those of R. nigrum are rectangular to almost round. Under the epidermis, in both fruits, there are two layers of oval hypodermal cells. Underneath the hypodermal layers,

parenchyma cells of different size with thin walls and scattered collateral closed bundles were detected. The

seeds are embedded in a gelatinous sheath having large thin-walled cells. Endocarp separates the arillar tissue from parenchyma cells, in addition, a gap can be found among these layers, endocarp, arillar tissue,

and seeds. The seed coat consists of sclerenchyma cells in both species. In conclusion, histological

differences and similarities were described in the fruits of the selected Ribes species, highlighted the first

morpho-anatomical description of the berry of Ribes rubrum.

Keywords: Ribes nigrum, Ribes rubrum, fruit, microscopic examination.

1. Introduction

Grossulariaceae family is composed of

approximately 195 species (The Plant List,

2018). According to Plant Database (USDA,

2018) there are 65 species of Ribes genus

including native and introduced plants in the

USA. In Europe 16 Ribes species are known

(Marhold, 2011; EU-NOMEN) involving 8

taxa in Romania namely R. uva-crispa L., R.

nigrum L., R. alpinum L., R. aureum Pursh, R.

sanguineum Pursh, R. petraeum Wulfen in

Jacq., R. spicatum Robson, and R. rubrum L.

(Ciocarlan, 2000). Ribes nigrum (black currant)

is a perennial shrub which grows in bushy

places, groves (Ciocarlan, 2000). It is also

widely cultivated for berry production. The

species has a wide variety of secondary

metabolites. Leaves contain lignoids (Sasaki et

al. 2013), glycosides of quercetin and

kaempferol as major phenolics (Liu et al.,

2014), accompanied by significant amounts of

salicylic acid, p-coumaric acid, caffeic and

gallic acids (Nour et al., 2014). Mineral and

Acta Biologica Marisiensis

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Eszter Laczkó-Zöld et al.

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trace elements also were measured in the leaves

of different cultivars of the plant (Nour et al.,

2014). Fruits contain phenolics: they are

especially rich in anthocyanins, e.g. glycosides

of delphinidin and cyanidin (Gavrilova et al.

2011). The level of anthocyanins varies

depending on the season, degree of maturity,

environmental conditions, type of cultivation,

and genetic characters (Milivojevic et al., 2012;

Zheng et al., 2012; Vagiri et al., 2013; Mikulic-

Petkovsek et al., 2015). Among organic acids,

citric, fumaric and malic acids are dominant

(Mikulic-Petkovsek et al., 2012; Woznicki et

al., 2017). The fruits are rich in vitamin C

(Häkkinen et al. 1999).

Ribes rubrum (red currant) is cultivated in

Romania, which is not the member of the

spontaneous flora (Ciocarlan, 2000). In the

literature it is known under synonymies R.

vulgare Lam. and R. sylvestre Mert. et Koch

(Ciocarlan, 2000; Marhold, 2011; EU-

NOMEN). In phytochemical aspect,

anthocyanin content – mostly glycosides of

cyanidin (Gavrilova et al., 2011; Mikulic-

Petkovsek et al., 2015) – is about 10% in the

fruit compared to that of black currant

(Gavrilova et al., 2011; Mikulic-Petkovsek et

al., 2015). Among flavonoids, glycosides of

quercetin, myricetin and kaempferol (Mikulic-

Petkovsek et al. 2015), as well as citric,

fumaric and malic acids were detected in the

plant in similar, but shikimic acid in 13 times

higher quantity compared to the fruit of black

currant (Mikulic-Petkovsek et al. 2012).

In the fruit of both species, fructose and

glucose are predominant among sugars

(Mikulic-Petkovsek et al., 2012; Woznicki et

al., 2017). The seed oil is rich in tocopherol,

unsaturated fatty acids, linoleic, α-linolenic,

and γ-linolenic acids (Traitler et al., 1984;

Goffman and Galetti, 2001; Leskinen et al.,

2009; Vuorinen et al., 2016).

In pharmacological aspect, currants were

studied for the effect in dietary management of

various diseases (Zágoni, 2005; Zdunić et al.,

2016). Polyphenolic substances of the fruit and

leaf were earlier examined for the anti-

inflammatory, antioxidant, antifungal, and

anticancer effect (Knekt et al., 1997; Šavikin et

al., 2009; Bishayee et al., 2010; Slavin and

Lloyd, 2012). The polyphenolic composition of

the fruit and the leaf of black currant plays a

role in the structure of biological and lipid

membranes, highlighted flavonols in the leaf,

and anthocyanins in the fruit as dominant

antioxidant compounds. The studied extracts

protected the membranes against the oxidation

and modified the properties of the hydrophilic

regions of the membranes (Cyboran et al.

2014). The fruits of black and red currant were

tested in vitro for potential management of type

2 diabetes and hypertension resulted high α-

glucosidase, α-amylase and ACE inhibitor

activities in red currant (Da Silva Pinto et al.,

2010).

Despite the described phytochemical and

pharmacological potential of the selected

species, there are few studies on the morpho-

anatomical description of the fruits as

medicinally used parts in Ribes species

(Wrońska-Pilarek, 2001; Wrońska-Pilarek,

2002; Kendir et al., 2015). In an earlier report

arrilar tissue was observed in several species of

the genus. Among them, arils cover the seeds in

the slightly fleshy pericarps in R. nigrum,

which is absent in R. rubrum (Corner, 1976).

In the last two decades, only one

histological report was published on the fruit of

black currant (Glidewell et al., 1999), and

according to our best knowledge no other

recent study is available concerning the

histology of red currant. Thus, this work aimed

to perform a comparative histological

characterization of the fruit of R. nigrum and R.

rubrum collected in Romania.


ABMJ 2019, 2(2): 5-14

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2. Materials and Methods

2.1 Plant material

Fruits of R. nigrum and R. rubrum (10

pieces of each species) were harvested at full

maturity from a local farmer’s garden in July

and August 2016 (Cornești, Mureș County,

Romania). Collected samples were frozen and

stored at -20°C until analyses.

2.2 Morphological and anatomical study

For microscopic examination, whole fruits

were preserved in the mixture of ethanol :

glycerine : distilled water (1:1:1). Fruits were

dehydrated in 50%, 70% and 96% ethanol

(Békési-Kallenberger et al. 2016), then they

were embedded in Technovit® 7100 resin

(Realtrade Ltd., Hungary). 15 µm thick cross-

sections were obtained with a rotary microtome

(Anglia Scientific 0325) (Papp et al., 2013).

The slides were dried at 50°C for 2 hours,

stained in toluidine blue (0.02%) for 5 min, and

soaked twice in 96% ethanol (3 min each),

isopropanol (4 min), and twice in xylol (3 and

4 min). Sections were studied with a NIKON

Eclipse 80i microscope and micrographs were

taken with SPOT Basic 4.0 image analysis

system.

3. Results and discussions

3.1 Histological features of the fruit of

Ribes nigrum

In the fruit of R. nigrum, the epidermis is

formed of rectangular to almost round shape

cells covered by cuticle layer. Under the

epidermis (epicarp), two layers of oval

hypodermal cells can be found (Fig. 1 A,B).

Under the hypodermal layers the mesocarp

parenchyma is composed of different size of

thin-walled cells and scattered vascular bundles

(Fig. 1 A,C). The collateral closed vascular

bundles consists of xylem and phloem that are

surrounded by sclerenchyma (Fig. 1 D). Seeds

are embedded in a gelatinous sheath which is

constructed from large thin-walled cells (Fig. 2

A,B,C), accordingly to a previous study

(Glidewell et al. 1999). The arillar tissue is

separated from the endocarp by a space (Fig. 2

B). The seed coat (testa) consists of

sclerenchyma cells (Fig. 2 D).

3.2 Histological features of the fruit of

Ribes rubrum

In R. rubrum, the epidermis of the fruit is

formed from more ovoid to round cells than

those of R. nigrum. The double-layered

hypodermis contains horizontally thick-walled

and elongated cells (Fig. 3 A, 3 D).

Parenchyma is composed of thin-walled cells in

various sizes. The scattered collateral closed

vascular bundles (Fig. 3 A) have only xylem

and phloem elements (Fig. 3 B). Endocarp

separates the arillar tissue from parenchyma

cells; between arillar tissue and seeds a gap was

observed (Fig. 3 C). Similar to black currant,

seeds are embedded in a gelatinous sheath (Fig.

3 C, Fig. 4 A) consisting of large cells with

slightly sinuous cell walls (Fig. 4 C). The seed

coat includes sclerenchyma cells (Fig. 4 B),

while the storage ground tissue consists of

thick-walled cells in the seed (Fig. 4 D).

Under histological aspect, the stem of

some Ribes species were described in wood

anatomical atlases (Metcalfe and Chalk, 1957;

Schweingruber et al. 2011), e.g. a diffuse-

porous xylem in Ribes nigrum (Schweingruber

et al. 2011). In another work, the whole fruit of

Ribes nigrum was analysed in different

developmental stages (Glidewell et al. 1999).

Morphological and histological characters of

the seed were reported for native species like R.

uva-crispa, R. alpinum, R. petraeum, and R.

spicatum in Poland (Wrońska-Pilarek, 2001;

Wrońska-Pilarek, 2002), as well as a surface

analysis by scanning microscope on the fruit,

seed and pollen of R. biebersteinii Berl. ex.

DC, R. uva-crispa, R. alpinum, R. orientale

Desf., R. multiflorum Kit. ex Romer &Schultes,

and R. anatolica Behcet which are native to



8

Turkey (Kendir et al., 2015), without detailed

histological description of all parts of the fruits.

Based on these studies, our work describes the

histological features of the whole fruit of Ribes

nigrum and R. rubrum including the seeds from

the collected samples from Romania. In this

work the fruit of red currant is described in all

details here for the first time. Similarities and

differences were observed in microscopic

preparations of the fruit of both currant species.

Among similar features, a thin layer of cuticle,

lack of stomata, two layers of hypodermal cells

(Fig. 1 B, 2 A), scattered collateral closed

bundles (Fig. 1 D, 3 B), and arillar tissue (Fig.

2 B) can be mentioned. The seed coats of both

species consist of sclerenchyma cells

surrounded by a gelatinous sheath (Fig. 1 C, 2

C) which is in accordance with earlier literature

data (Glidewell et al. 1999). This sheath, also

called sarcotesta, is different in thickness in

Ribes species. Sometimes it is equal to the

width of the seeds (Wrońska-Pilarek, 2001),

but it is less than half of those in R. nigrum and

R. rubrum described in this study. In both

fruits, major part of the pericarp and the

placental region is occupied by medium and

large parenchyma cells (Fig. 1 A,C and Fig. 3

A,C,D), as it was previously described in black

currant (Glidewell et al. 1999).

Fig. 1. Histological features of the fruit of Ribes nigrum. A-B) fruit wall; C) seed embedded in

gelatinous sheath; D) collateral closed vascular bundle; e: epicarp (epidermis), ec: endocarp,

ch: collenchymatic hypodermis, gs: gelatinous sheath, m: mesocarp, xy: xylem, ph: phloem,

sc: sclerenchyma, sd: seed, vb: vascular bundle


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Fig. 2. Histological features of the seed of Ribes nigrum. A) seed; B) aril; C) gelatinous cells;

D) testa; ar: aril, eb: the place of embryo (tissue is missing), ec: endocarp, es: endosperm,

gs: gelatinous sheath, pc: parenchyma cells, sc: sclerenchyma cells, sd: seed

Fig. 3. Histological features of the fruit of Ribes rubrum. A) pericarp; B) vascular bundle; C) seed

embedded in gelatinous sheath; D) pericarp; e: epicarp (epidermis), ec: endocarp,

ch: collenchymatic hypodermis, gs: gelatinous sheath, m: mesocarp, xy: xylem, ph: phloem,

sd: seed, vb: vascular bundle



10

As differences, various shapes of

epidermis cells (Fig. 1 B, 3 A) and different

intensity of dyeing of parenchymal cells were

observed: stronger coloration of the pericarp

and placenta refer to a higher polysaccharide

content in black currant compared to red

currant (Fig. 1 A, 3 A,C). Contrary to

gooseberry’s fruit (Williamson et al., 1993), the

gelatinous sheath around the seeds is not

single-layered, but multi-layered up to six cell

layers in the studied species (Fig. 1 C, 4 A). In

the endosperm, fatty oil drops were detected in

R. nigrum (Fig. 2 D), which does not appear in

R. rubrum (Fig. 4 D). This is in accordance

with earlier findings using Sudan IV:

coloration was found only in the external layer

of the endosperm in red currant (Wrońska-

Pilarek 2001).

Generally, in berries (Giongo et al. 2013),

as in other fruits such as tomato (Saladie et al.

2007), the texture of the fruit is related to the

cell wall structure and to change in ripening

phases (Giongo et al. 2013). The structure of

the pericarp has a great influence on the storage

ability of the ripe fruit and the postharvest

management. As expected, epidermal cells in

the berry of black and red currant are covered

by cuticle which can explain the relative long

maintenance of their freshness.

Fig. 4. Histological features of the seed of Ribes rubrum. A) Seed embedded in gelatinous sheath;

B) seed; C) gelatinous sheath; D) endosperm; eb: the place of embryo (tissue is missing),

gs: gelatinous sheath, sc: sclerenchyma cells, sd: seed


ABMJ 2019, 2(2): 5-14

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Conclusions

The histological determination of the

fruit of Ribes nigrum and R. rubrum complete

the reported data of the species. In the fruits

of the selected Ribes species differences and

similarities are described, which highlight the

first morpho-anatomic study of the fruit of

Ribes rubrum. The observed features play an

important role in the characterisation, which

will be useful providing a reliable basis for

identification of the fruits.

Conflict of Interest

The authors declare that the research was

conducted in the absence of any commercial

or financial relationships that could be

construed as a potential conflict of interest.

Acknowledgments

The study was supported by the Research

Grant of the University of Pécs (PTE ÁOK

KA-2017-27), grant from OTKA (K 127944),

and the Research Grant of Studium Prospero

Foundation (0350/26.02.2016)

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Acta Biologica Marisiensis COMPARATIVE HISTOLOGICAL ...€¦ · Ribes nigrum (black currant) is a perennial shrub which grows in bushy places, groves (Ciocarlan, 2000). It is also